Lepidoptera: Nymphalidae: Biblidinae)

Home , Biblidinae, Dalechampia triphylla, Dynamine, Hamadryas (butterfly), Hamadryas amphinome, Hamadryas feronia

Revista Brasileira de Entomologia 59 (2015) 301–306

REVISTA BRASILEIRA DE

Entomologia

A Journal on Insect Diversity and Evolution

w ww.rbentomologia.com

Systematics, Morphology and Biogeography

Immature stages of Hamadryas fornax fornax (Hübner) (Lepidoptera:

Nymphalidae: Biblidinae)

a,∗ b a

Lucy Mila Garcia Salik , Luis Anderson Ribeiro Leite , Fernando Maia Silva Dias ,

a a

Mirna Martins Casagrande , Olaf Hermann Hendrik Mielke

Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, PR, Brazil

Laboratório de Entomologia, Departamento de Biologia, Universidade Federal de Sergipe, São Cristóvão, SE, Brazil

a b s

r a c t

a r t i c l e i n f o

Article history: The external morphology and biology of the immature stages of Hamadryas fornax fornax (Hübner, [1823])

Received 12 August 2014

(Lepidoptera, Nymphalidae, Biblidinae) recorded on Dalechampia triphylla (Euphorbiaceae) in Curitiba,

Accepted 4 August 2015

Paraná, Brazil are described. Morphological characters are illustrated and described, as a result of obser-

Available online 1 October 2015

vations in scanning electron, stereoscope and optical microscopes, the last two attached to a camera

Associate Editor: Luis Parra

lucida. Results are compared and discussed with immature stages of other species of Biblidinae.

Keywords:

Bionomy access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Life cycle Neotropical

Papilionoidea

Introduction on the ventral side of the hind wing (Jenkins, 1983). Immatures

are associated to plants of the genus Dalechampia (Euphorbiaceae)

Hamadryas Hübner, [1806] (Lepidoptera: Nymphalidae: Biblid- (D’Almeida, 1922; Costa Lima, 1936; Armbruster, 1982, 1983;

inae) encompasses 20 species and 33 subspecies (Lamas, 2004); Jenkins, 1983; Neild, 1996; Canals, 2003; Pastrana, 2004). Females

these butterﬂies are popularly known as crackers, due to the are similar to males, but frequently with larger size and forewings

characteristic noise some species produce while ﬂying (Jenkins, with a more rounded shape (Figs. 1–4) (Jenkins, 1983).

1983; Otero, 1991; Monge-Nájera, 1992, 1995; Monge-Nájera and Despite the large amount of data on the geographic distri-

Hernández, 1993; Monge-Nájera et al., 1998; Yack et al., 2000; bution and host plants found in the literature (Jenkins, 1983;

Marini-Filho and Benson, 2010; Murillo-Hiller, 2011). They are DeVries, 1987; Neild, 1996; Pastrana, 2004; Contreras Chialchia

restricted to the Americas and occur in tropical and subtropi- and Contreras Roqué, 2010), currently there is information on

cal forests, savannas, arid and semi-arid lands (Jenkins, 1983). the morphology and biology of immature stages of only eight

Hamadryas fornax (Hübner, [1823]) has two recognized subspecies species: H. feronia feronia (Linnaeus, 1758), (D’Almeida, 1922); H.

(Lamas, 2004): H. fornax fornax (Hübner, [1823]) with South amphinome amphinome (Linnaeus, 1767) (D’Almeida, 1922; Müller,

American distribution from Venezuela to Argentina and H. fornax 1886; Muyshondt and Muyshondt, 1975a); H. fornax fornax (Hüb-

fornacalia (Fruhstorfer, 1907) distributed from the South of United ner, [1823]) (Müller, 1886); H. februa februa (Hübner, [1823])

States to the Northern part of Colombia and Venezuela (DeVries, (Comstock and Vasquez Garcia, 1961; D’Almeida, 1922; Muyshondt

1987; Jenkins, 1983; Neild, 1996; Lamas, 2004). and Muyshondt, 1975b; Young, 1974); H. arete (Doubleday, 1847)

Hamadryas fornax fornax (Hübner, [1823]) usually perches (Müller, 1886); H. guatemalena guatemalena (H. W. Bates, 1864)

upside down on tree trunks on valleys of rivers and clearings in for- (Muyshondt and Muyshondt, 1975c) and H. epinome (C. Felder

est habitats and despite its similarity with the other species of the & R. Felder, 1867) (Müller, 1886; D’Almeida, 1922; Leite et al.,

genus, it is distinguished by its forewing on the ventral surface with 2012b).

the proximal area of the discal cell presenting white or grayish- It is widely known that data on the immature stages are impor-

white coloration, rarely pale-yellow and the mustard coloration tant for taxonomic and phylogenetic studies of Lepidoptera (Freitas

et al., 1997; Freitas and Brown, 2004); therefore this study aims to

provide information and extend the knowledge on the subfamily ∗

Corresponding author.

E-mail: [email protected] (L.M.G. Salik).

http://dx.doi.org/10.1016/j.rbe.2015.08.002

0085-5626/© 2015 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

302 L.M.G. Salik et al. / Revista Brasileira de Entomologia 59 (2015) 301–306

Figs. 1–4. Hamadryas fornax fornax (Hübner, [1823]). 1, 2. Male: 1, dorsal view; 2, ventral view; 3, 4. Female: 3, dorsal view; 4, ventral view. Scale bar: 1 cm.

Biblidinae by describing the external morphology and the biology same color of the pronotal plate. Body translucent yellowish ochre,

of the immature stages of H. fornax fornax. with rounded white spots regularly distributed on the dorsal and

lateral areas. Numerous spiniform or clavate black setae distributed

along the body, most of them on chalazae. Bases of all black setae

Material and methods

forming circular blackened areas interspersed with white rounded

◦

areas. Spiracles of T1 and A8 elliptical and similar; other spiracles

Eggs were collected in the Parque Municipal Barigui (25 25 S,

◦

smaller and rounded. After the eclosion, the larvae are not gregar-

49 18 W, 910 m), Curitiba, Paraná, Brazil, along with branches

ious, and feed independently. Chaetotaxy is given by Figs. 19–21.

of the host plant Dalechampia triphylla Lam. (Euphorbiaceae)

Head capsule: width: 0.65 mm; height: 0.68 mm. Average length

and reared in laboratory (Laboratório de Estudos de Lepidoptera

of the larva before molting: 5 mm. Average duration: 3 days (n = 9).

Neotropical at the Universidade Federal do Paraná). Laboratory pro-

cedures, such as the maintenance of the samples and the host plant,

preparation and observation of the structures using stereoscopic

Second instar (Figs. 11, 23)

microscope, drawings, photographs, scanning electron microscopy

Head capsule black. Epicranium with a pair of short truncated

and terminology follows Leite et al. (2012b) and other recent stud-

dorsal scoli. Setae on lateral and lateroventral regions of the epi-

ies on immatures of Biblidinae (Leite et al., 2012a, 2014). Voucher

cranium on cream-colored chalazae. Prothorax yellow ochre, with

specimens are deposited at the Colec¸ ão Entomológica Pe. Jesus

black and distally creamy white scoli. Remaining segments olive

Santiago Moure; Universidade Federal do Paraná, Curitiba, Paraná,

brown with a narrow yellow ochre lateral band in A1–A10, at the

Brazil.

level of the supraventral setae. Thorax and abdomen with subdor-

sal black and distally creamy white scoli on T2, T3, A7 and A8,

Results remaining scoli translucent yellow.

Head capsule: width: 1.04 mm, height: 0.95 mm. Length of the

Hamadryas fornax fornax (Hübner, [1823]) (Figs. 1–29) dorsal protuberance: 0.44 mm. Average length of the larva before

molting: 6 mm. Average duration: 3 days (n = 8).

Egg (Figs. 5–9)

Elliptical, with several irregular carinae and ﬂattened on the bot-

Third instar (Figs. 12, 24)

tom pole. Uniformly pearly white in color. Micropilar region on the

Head capsule black; dorsal scoli longer than the previous instar,

upper pole in the center of a round and slightly concave area.

blackened and with spiniform setae. Thorax and abdomen with the

Oviposition is normally gregarious; the eggs are laid on the

same coloration of the head, except for the yellow ochre supraven-

upper side of the host plant Dalechampia triphylla, one on top of

tral and ventral areas. Most of the thoracic and abdominal scoli

each other, the ﬁrst instar hatch laterally.

black, except for some lateral translucent yellow scoli from A3 to

Diameter: 1.01 mm. Average duration: 8 days (n = 15).

A6.

Head capsule: width: 1.63 mm; height: 1.66 mm. Length of the

First instar (Figs. 10, 19–22)

dorsal protuberance: 2.7 mm. Average length of the larva before

Head rounded, black, and without scoli. Frons ventrally delim-

molting: 13.5 mm. Average duration: 4 days (n = 7).

ited by the clypeus, which appears as a sclerotized transverse band.

Labrum bilobed. Mandibles strongly sclerotized with a serrated cut-

ting edge. Six stemmata latero-ventrally, 1–4 and 6 arranged in Fourth instar (Figs. 13, 25)

semi-circle and 5 ventrally, and closer to the base of the antenna. Head capsule similar to the previous instar. Prothorax anteri-

Pronotal plate black and divided, forming two sub-rectangular orly reddish-brown, with black pronotal plate. Dorsally, two pairs

plates, with four pairs of setae on chalazae. Thoracic legs with the of yellow longitudinal bands from T2 to A9. Reddish-brown band

L.M.G. Salik et al. / Revista Brasileira de Entomologia 59 (2015) 301–306 303

Figs. 5–18. Hamadryas fornax fornax (Hübner, [1823]). 5–9. Egg: 5, SEM lateral view; 6, SEM lateral view of the egg-laying; 7, lateral view; 8, dorsal view; 9, lateral view of

the egg-laying. 10–15. Larvae: 10, 1st instar; 11, 2nd instar; 12, 3rd instar; 13, 4th instar; 14, 5th instar lateral view; 15, 5th instar dorsal view. 16–18. Pupae: 16, ventral

view; 17, dorsal view; 18, lateral view. SEM – Scanning Electronic Microscopy. Scale bars Figs. 7–8: 0.5 mm, Fig. 9: 1 mm.

laterally disposed on T2 and T3 and on the abdominal segments at tudinal bands and an orange lateral band from the spiracular to the

the level of the supraventral setae. ventral area. Abdominal legs orange.

Head capsule: width: 1.8 mm, height: 1.7 mm. Length of the Head capsule: width: 3.4 mm, height: 3.2 mm. Length of the

dorsal protuberance: 3.2 mm. Average length of the larva before dorsal protuberance: 6.38 mm. Average length of the larva before

molting: 23 mm. Average duration: 4 days (n = 7). molting: 33 mm. Average duration: 7 days, 1 more day on prepupa

(n = 7).

Fifth instar larva (Figs. 14, 15 and 26)

Head capsule dark brown. Pronotal plate black. Spiniform setae Pupa (Figs. 27–29)

distributed along the body, sometimes grouped in scoli, some- Adecticous and obtect, suspended by the cremaster. Elongated,

times individualized, light brown setae, except those from the median-dorsally projected on T2 and A2, forming crests. Freshly

supraventral and ventral regions from T1 to A8, which have yellow formed pupae light green, darkening to brownish dark green in

coloration. Thorax and abdomen yellow, with several black longi- about one day. Light green semicircular spot dorsolaterally on T2.

304 L.M.G. Salik et al. / Revista Brasileira de Entomologia 59 (2015) 301–306

D1 D1 D1 D1 D2 D2 D2 D2 XDI XD2 SD1 SD2 SD2 SD1 SD1 D1 A8 A9+10 SD1 T1 T2 T3 A1 A2 A3 A4 A5 A6 A7 SD1 D2

L2 L1 SD2 L1 PP SV2 L2 L1 L1 SV1 SV1 SV1 SV2 SV1 L1 SV1 SV1 L2 SV1 SV2 SV1 SV4 SV3 V1 SV2 L3 V1 V1 V1 19

D1 XD1 D1 XD2

SD1

D2 D2

20SD2 21

Figs. 19–21. Hamadryas fornax fornax (Hübner, [1823]). 1st instar chaetotaxy: 19, map of setae of the thorax and abdomen; 20, pronotal plate; 21, anal plate.

Figs. 25–26. Hamadryas fornax fornax (Hübner, [1823]). Head capsule frontal view:

25, 4th instar; 26, 5th instar; 24. Scale bar Fig. 25: 0.5 mm; Fig. 26: 1 mm.

arising inferiorly to the mandibles and lateroinferiorly to the

labrum and ending next to the distal portion of the antennae; eyes

laterally to the mandibular region; striated antennae extendly, lat-

eral to the eyes, proximal portion at the base of the foliaceous

Figs. 22–24. Hamadryas fornax fornax (Hübner, [1823]). Head capsule frontal view:

appendices and distal portion on the forewing margins.

22, 1st instar; 23, 2nd instar; 24, 3rd instar. Scale bar Figs. 22, 23: 0.25 mm; Fig. 24:

0.5 mm. Pronotum subrectangular and small, with a median suture.

Mesonotum large and convex. Metanotum narrow, with a convex

A pair of foliaceous dorsolateral appendices on the head vertex. margin on its anteromedian region. Base of the prothoracic legs at

Frons smooth, subtriangular clypeus; mandibles lateroventrally to the inferior portion of the eye, laterally to the galeae and ending on

the clypeus; labrum as a small lozenge shaped structure inferi- the anterior half of these last ones; base of the mesothoracic legs on

orly to the clypeus and between the mandibles; dark brown galeae the anterior third of the antennae and ending at its posterior third.

L.M.G. Salik et al. / Revista Brasileira de Entomologia 59 (2015) 301–306 305

Figs. 27–29. Hamadryas fornax fornax (Hübner, [1823]). Pupa: 27, lateral view; 28, ventral view; 29, dorsal view. Scale bar: 0.5 cm.

Abdomen with ten segments, lateral elliptical spiracles from A2 Ageroniini, Batesia C. Felder and R. Felder, 1862 and Panacea God-

to A8. Narrow median dark brown band ventrally from A4 to A8. man and Salvin, 1883 do not have these projections (DeVries et al.,

Cremaster dark brown, with distal simple hooks on the apex of A10. 2000; Daniels et al., 2008). In Epiphilini, species of Temenis Hübner,

Average length of the pupa, from the vertex to the cremaster: [1819] (Muyshondt, 1974) also have these extensions, although not

30 mm. Average length of the foliaceous appendices: 15 mm. Aver- as long as in Hamadryas; other species of Biblidinae often have a

age duration: 7 days (n = 6). slightly pronounced vertex (i.e. DeVries, 1987), but never greatly

extended as the above-cited taxa. The dorsolateral color of T2 of

the pupae differentiates H. fornax fornax from H. epinome (Leite,

Discussion

2012b), which are lime green in the former and brown in the latter.

The current understanding of the phylogenetic relationships

Species of Hamadryas feed on species of Dalechampia, and D.

of Hamadryas (Garzón-Orduna,˜ 2012; Garzón-Orduna˜ et al., 2013)

tryphilla is recorded as host plant of H. fornax and further eight

lack morphological and biological evidence from immature stages

species of the genus (Beccaloni et al., 2008). Records of species

of potential evolutionary importance, such as the above-mentioned

of Hamadryas feeding on other genera of host plants provided by

differences in egg gregariousness, chaetotaxy, and scoli distribu-

Beccaloni et al. (2008) are unlikely and need conﬁrmation.

tion, for example. Unfortunately, most descriptions of immature

Biblidinae usually present eggs with well deﬁned crests, as in

stages of Hamadryas are brief, which limits comparisons. Studies

species of Temenis laothoe liberia (Fabricius, 1793) (Muyshondt,

like this are essential to provide a new array of characters for phy-

1974), Dynamine Hübner, [1819] (Leite et al., 2012a, 2014) and

logeny and a better understanding the systematic of the genus.

some species of Ageroniini, Panacea Godman and Salvin, 1883 and

Batesia C. Felder and R. Felder, 1862 (DeVries et al., 2000; Daniels

et al., 2008). In contrast, species of Hamadryas, such as H. fornax for-

Conﬂicts of interest

nax and H. epinome (Leite et al., 2012b) present eggs with irregular

ornamentation of the chorion, indicating that this character might

The authors declare no conﬂicts of interest.

be characteristic of the genus. In the ﬁrst instar, the shape of the

base of SD1 and SD2 on T1, T2 and T3, and the localization of D2 on

the pronotal plate differ from those found in H. epinome (Leite et al.,

Acknowledgments

2012b). In the ﬁfth instar, similar to H. guatemalena, H. februa, and

H. amphinome (Muyshondt and Muyshondt, 1975a,b,c), H. fornax

We would like to thank the Centro de Microscopia Eletrônica

fornax presents dorsal scoli only on A7 and A8, with three and ﬁve

(CME-UFPR) and the TAXon line – Rede Paranaense de Colec¸ ões

branches respectively. In H. epinome (Müller, 1886; Jenkins, 1983;

Biológicas of the Universidade Federal do Paraná for some of the

Leite et al., 2012b) additional dorsal scoli are present in all abdomi-

photographs; members of the Laboratório de Estudos em Lep-

nal segments, although simple and smaller than the those in A7 and

idoptera Neotropical (LELN-UFPR) for additional help; and the

A8 and the subdorsal scoli. Hamadryas (Muyshondt and Muyshondt,

Conselho Nacional de Desenvolvimento Cientíﬁco e Tecnológico

1975a,b,c) and Ectima Doubleday, [1848] (Janzen, 2010) present

(CNPq) for the fellowship granted to the authors.

long foliaceous projections on the vertex of the pupa. Pupae of other

306 L.M.G. Salik et al. / Revista Brasileira de Entomologia 59 (2015) 301–306

References Leite, L.A.R., Dias, F.M.S., Carneiro, E., Casagrande, M.M., Mielke, O.H.H., 2012b. Imma-

ture stages of the Neotropical cracker butterﬂy Hamadryas epinome. J. Insect Sci.

Armbruster, W.S., 1982. Seed production and dispersal in Dalechampia (Euphor- 12, 1–12.

biaceae): divergent patterns and ecological consequences. Am. J. Bot. 69, Leite, L.A.R., Freitas, A.V.L., Barbosa, E.P., Casagrande, M.M., Mielke, O.H.H., 2014.

1429–1440. Immature stages of nine species of genus Dynamine Hübner, [1819]: morphol-

Armbruster, W.S., 1983. Dalechampia scandens (Ortiguilla, Bejuco de Pan). In: Janzen, ogy and natural history (Lepidoptera: Nymphalidae: Biblidinae). SHILAP – Rev.

D.H. (Ed.), Costa Rican Natural History. The University of Chicago Press, Chicago, Lepidoptera 42, 27–55.

pp. 230–233. Marini-Filho, O.J., Benson, W.W., 2010. Use of sound and aerial chases in sexual

Beccaloni, G.W., Hall, S.K., Viloria, A.L., Robinson, G.S., 2008. Catalogue of the host- recognition in Neotropical Hamadryas butterﬂies (Nymphalidae). J. Res. Lepi-

plants of the Neotropical butterﬂies (Catálogo de las plantas huésped de las doptera 42, 5–12.

mariposas neotropicales). Mongr. Terc. Milênio 8, 1–536. Monge-Nájera, J., 1992. Clicking butterﬂies, Hamadryas, of Panama: their biology

Canals, G.R., 2003. Mariposas de Misiones. Literature of Latin America, Buenos Aires. and identiﬁcation (Lepidoptera: Nymphalidae). In: Quintero, D., Aiello, A. (Eds.),

Comstock, J.A., Vasquez Garcia, L., 1961. Estudios de los Ciclos Biologicos en Lepi- Insects of Panama and Mesoamerica. Selected Studies. Oxford University Press,

dopteros Mexicanos. An. I. Biol. 31, 349–448. Oxford, pp. 567–572.

Contreras Chialchia, A.O., Contreras Roqué, J.R., 2010. Presencia del género Monge-Nájera, J., 1995. Mariposas que producen sonido: cuál es la situación de

Hamadryas Hübner, 1825 (Lepidoptera: Nymphalidae: Biblidinae), en la Ecor- Hamadryas (Nymphalidae) en Cuba? Cocuyo 4, 11.

región del Neembucú˜ y en el resto del Paraguay Oriental. Azariana 1, Monge-Nájera, J., Hernández, F., 1993. A morphological search for the sound mech-

225–242. anism of Hamadryas butterﬂies (Lepidoptera: Nymphalidae). J. Res. Lepidoptera

Costa Lima, A.C., 1936. Terceiro Catálogo de insectos que vivem nas plantas do Brasil. 30, 196–208.

Escola Nacional de Agronomia, Rio de Janeiro. Monge-Nájera, J., Hernández, F., González, M.I., Soley, J., Araya, J., Zolla, S., 1998.

D’Almeida, R.F., 1922. Mélanges Lépidoptérologiques. Études sur les Lépidoptères Spatial distribution, territoriality and sound production by tropical cryptic but-

du Brésil. Friedländer and Sohn, Berlin. terﬂies (Hamadryas, Lepidoptera: Nymphalidae): implications for the “industrial

Daniels, J.C., Rodriguez, E., Whelan, J.C., 2008. The biology and immature stages of melanism” debate. Rev. Biol. Trop. 46, 297–329.

Panacea procilla lysimache (Lepidoptera: Nymphalidae) from Costa Rica, with Müller, W., 1886. Südamerikanische Nymphalidenraupen. Versuch eines natür-

report of a new locality record. Trop. Lepid. 18, 70–73. lichen Systems der Nymphaliden. Zool. Jahrb. (Syst.) 1, 453–461.

DeVries, P.J., 1987. The Butterﬂies of Costa Rica and their natural history: Papilion- Murillo-Hiller, L.R., 2011. The spiral organ responsible for producing sound sig-

idae, Pieridae, and Nymphalidae. Princeton University Press, Princeton. nals, an essential taxonomic character in the phylogenetic analysis of the genus

DeVries, P.J., Penz, C.M., Walla, T.R., 2000. The biology of Batesia hypochlora in an Hamadryas (Nymphalidae: Biblidinae): the case of Hamadryas chloe chloe (Stoll)

Ecuadorian rainforest. Trop. Lepid. 10, 43–46. [1787] from South America. Int. Sch. Res. Net Zool., 1–3.

Freitas, A.V.L., Brown Jr., K.S., Otero, L.D., 1997. Juvenile stages of Cybdelis, a key genus Muyshondt, A., 1974. Notes on the life cycle and natural history of butterﬂies of El Sal-

uniting the diverse branches of the Eurytelinae. Trop. Lepid. 8, 29–34. vador. III.A. Temenis laothoe liberia Fabricius (Nymphalidae – Catonephelinae). J.

Freitas, A.V.L., Brown Jr., K.S., 2004. Phylogeny of the Nymphalidae (Lepidoptera). N. Y. Entomol. Soc. 81, 224–233.

Syst. Biol. 53, 363–383. Muyshondt, A., Muyshondt Jr., A., 1975a. Notes on the life cycle and natural his-

Garzón-Orduna,˜ I.J., 2012. Phylogenetic evidence for loss of sound production and tory of butterﬂies of El Salvador. III.B. Hamadryas amphinome L. (Nymphalidae –

a shift in sexual recognition signals in Hamadryas butterﬂies (Nymphalidae: Hamadryadinae). J. N. Y. Entomol. Soc. 83, 181–191.

Biblidinae). Syst. Entomol. 37, 84–101. Muyshondt, A., Muyshondt Jr., A., 1975b. Notes on the life cycle and natural history of

Garzón-Orduna,˜ I.J., Marini-Filho, O., Johnson, S.G., Penz, A.M., 2013. Phylo- butterﬂies of El Salvador. I.B. – Hamadryas februa (Nymphalidae – Hamadryadi-

genetic relationships of Hamadryas (Nymphalidae: Biblidinae) based on nae). J. N. Y. Entomol. Soc. 83, 157–169.

the combined analysis of morphological and molecular data. Cladistics 29, Muyshondt, A., Muyshondt Jr., A., 1975c. Notes on the life cycle and natural history

629–642. of butterﬂies of El Salvador. II B. – Hamadryas guatemalena Bates (Nymphalidae

Janzen, D.H., Hallwachs, W., 2010. Dynamic database for an inventory of – Hamadryadinae). J. N. Y. Entomol. Soc. 83, 170–180.

the macrocaterpillar fauna, and its food plants and parasitoids, of Area Neild, A.F.E., 1996. The Butterﬂies of Venezuela. Part I: Nymphalidae (Limenitidinae,

de Conservacion Guanacaste (ACG), northwestern Costa Rica, Available at: Apaturinae, Charaxinae). Meridian Publications, London.

http://janzen.sas.upenn.edu (accessed 05.08.15). Otero, L.D., 1991. The stridulatory organ in Hamadryas (Nymphalidae): preliminary

Jenkins, D.W., 1983. Neotropical Nymphalidae. I. Revision of Hamadryas. Bull. Allyn. observations. J. Lepid. Soc. 44, 285–288.

Mus. 81, 1–146. Pastrana, J.A., 2004. Los lepidópteros argentinos: sus plantas hospedadoras y otros

Lamas, G., 2004. Checklist: part 4A. Hesperioidea – Papilionoidea. In: Heppner, J.B. sustratos alimenticios. Sociedad Entomológica Argentina, Buenos Aires.

(Ed.), Atlas of Neotropical Lepidoptera, vol. 5A. Association for Tropical Lepi- Yack, J.E., Otero, L.D., Danson, J.W., Surlykke, A., Fullard, J., 2000. Sound produc-

doptera, Scientiﬁc Publishers, Gainesville, pp. 238–239. tion and hearing in the blue cracker butterﬂy Hamadryas feronia (Lepidoptera,

Leite, L.A.R., Casagrande, M.M., Mielke, O.H.H., Freitas, A.V.L., 2012a. Immature Nymphalidae) from Venezuela. J. Exp. Biol. 203, 3689–3702.

stages of the Neotropical butterﬂy Dynamine agacles agacles. J. Insect Sci. 12, Young, A.M., 1974. On the biology of Hamadryas februa (Lepidoptera: Nymphalidae)

1–12. in Guanacaste, Costa Rica. Z. Angew. Entomol. 76, 380–393.